Timing and location of speech errors induced by direct cortical stimulation

Abstract

Cortical regions supporting speech production are commonly established using neuroimaging techniques in both research and clinical settings. However, for neurosurgical purposes, structural function is routinely mapped peri-operatively using direct electrocortical stimulation. While this method is the gold standard for identification of eloquent cortical regions to preserve in neurosurgical patients, there is lack of specificity of the actual underlying cognitive processes being interrupted. To address this, we propose mapping the temporal dynamics of speech arrest across peri-sylvian cortices by quantifying the latency between stimulation and speech deficits. In doing so, we are able to distinguish functional roles (e.g., planning versus motor execution). In this retrospective observational study, we analyzed 20 patients (12 female; age range 14-43) with refractory epilepsy who underwent continuous extra-operative intracranial EEG monitoring during an automatic speech task during clinical bed-side language mapping. Latency to speech arrest was calculated as time from stimulation onset to speech arrest onset, controlling for individuals' speech rate. Most motor-based interruptions (87.5% of 96 instances) were in motor cortex with mid-range latencies to speech arrest (median = 0.79 s, 95% CI = 0.55-0.92 s). Speech arrest occurred in numerous regions, with short latencies in supramarginal gyrus (median = 0.49 s, 95% CI = 0.41-0.61 s), superior temporal gyrus (median = 0.55 s, 95% CI = 0.45-0.66 s), and middle temporal gyrus (median = 0.57, 95% CI = 0.43-0.79 s), followed by motor cortex (median = 0.83 s, 95% CI = 0.70-1.17 s) and inferior frontal gyrus (median = 0.90 s, 95% CI = 0.74-0.95 s). Nonparametric testing for speech arrest revealed that region predicted latency, χ^2 "(4)" = 28.798, p < 0.00001; latencies in supramarginal gyrus and in superior temporal gyrus were shorter than in motor cortex (D = 0.48, p = 0.00011; D = 0.38, p = 0.004) and in inferior frontal gyrus (D = 0.46, p < 0.00001; D = 0.35, p = 0.00095). Motor cortex is primarily responsible for motor-based speech interruptions. Latencies to speech arrest in supramarginal gyrus and superior temporal gyrus align with latencies to motor-based speech interruptions in motor cortex, suggesting that stimulating these regions interferes with the outgoing motor execution. The longer latencies to speech arrest in inferior frontal gyrus and in ventral regions of motor cortex suggest that stimulating these areas interrupts planning. These results implicate the ventral specialization of motor cortex for speech planning above and beyond motor execution.